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Title: Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility

Abstract

Plant biomass is a large source of fermentable sugars for the synthesis of bioproducts using engineered microbes. These sugars are stored as cell wall polymers, mainly cellulose and hemicellulose, and are embedded with lignin, which makes their enzymatic hydrolysis challenging. One of the strategies to reduce cell wall recalcitrance is the modification of lignin content and composition. Lignin is a phenolic polymer of methylated aromatic alcohols and its synthesis in tissues developing secondary cell walls is a significant sink for the consumption of the methyl donor S-adenosylmethionine (AdoMet). In this study, we demonstrate in Arabidopsis stems that targeted expression of AdoMet hydrolase (AdoMetase, E.C. 3.3.1.2) in secondary cell wall synthesizing tissues reduces the AdoMet pool and impacts lignin content and composition. In particular, both NMR analysis and pyrolysis gas chromatography mass spectrometry of lignin in engineered biomass showed relative enrichment of non-methylated p-hydroxycinnamyl (H) units and a reduction of dimethylated syringyl (S) units. This indicates a lower degree of methylation compared to that in wild-type lignin. Quantification of cell wall-bound hydroxycinnamates revealed a reduction of ferulate in AdoMetase transgenic lines. Biomass from transgenic lines, in contrast to that in control plants, exhibits an enrichment of glucose content and a reductionmore » in the degree of hemicellulose glucuronoxylan methylation. We also show that these modifications resulted in a reduction of cell wall recalcitrance, because sugar yield generated by enzymatic biomass saccharification was greater than that of wild-type plants. Considering that transgenic plants show no important diminution of biomass yields, and that heterologous expression of AdoMetase protein can be spatiotemporally optimized, this novel approach provides a valuable option for the improvement of lignocellulosic biomass feedstock.« less

Authors:
 [1];  [2];  [3];  [1];  [1];  [1];  [2];  [1];  [4];  [1];  [2];  [5];  [6]
  1. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division
  2. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering, Dept. of Chemical and Biomolecular Engineering
  3. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Univ. of California, Berkeley, CA (United States). Dept. of Bioengineering, Dept. of Chemical and Biomolecular Engineering; Univ. of Louisville, KY (United States). Dept. of Chemical Engineering
  4. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  5. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Sandia National Lab. (SNL-CA), Livermore, CA (United States)
  6. Joint BioEnergy Inst. (JBEI), Emeryville, CA (United States); Lawrence Berkeley National Lab. (LBNL), Berkeley, CA (United States). Biological Systems and Engineering Division; Claude Bernard Uni., Villeurbanne (France)
Publication Date:
Research Org.:
Lawrence Berkeley National Laboratory (LBNL), Berkeley, CA (United States)
Sponsoring Org.:
USDOE Office of Science (SC), Biological and Environmental Research (BER); National Science Foundation (NSF)
OSTI Identifier:
1378985
Grant/Contract Number:  
AC02-05CH11231; 1355438
Resource Type:
Journal Article: Accepted Manuscript
Journal Name:
Frontiers in Bioengineering and Biotechnology
Additional Journal Information:
Journal Volume: 4; Journal ID: ISSN 2296-4185
Publisher:
Frontiers Research Foundation
Country of Publication:
United States
Language:
English
Subject:
37 INORGANIC, ORGANIC, PHYSICAL, AND ANALYTICAL CHEMISTRY; 09 BIOMASS FUELS; cell wall; lignin; S-adenosylmethionine; AdoMetase; Yang cycle; glucuronoxylan; saccharification

Citation Formats

Eudes, Aymerick, Zhao, Nanxia, Sathitsuksanoh, Noppadon, Baidoo, Edward E. K., Lao, Jeemeng, Wang, George, Yogiswara, Sasha, Lee, Taek Soon, Singh, Seema, Mortimer, Jenny C., Keasling, Jay D., Simmons, Blake A., and Loqué, Dominique. Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility. United States: N. p., 2016. Web. doi:10.3389/fbioe.2016.00058.
Eudes, Aymerick, Zhao, Nanxia, Sathitsuksanoh, Noppadon, Baidoo, Edward E. K., Lao, Jeemeng, Wang, George, Yogiswara, Sasha, Lee, Taek Soon, Singh, Seema, Mortimer, Jenny C., Keasling, Jay D., Simmons, Blake A., & Loqué, Dominique. Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility. United States. https://doi.org/10.3389/fbioe.2016.00058
Eudes, Aymerick, Zhao, Nanxia, Sathitsuksanoh, Noppadon, Baidoo, Edward E. K., Lao, Jeemeng, Wang, George, Yogiswara, Sasha, Lee, Taek Soon, Singh, Seema, Mortimer, Jenny C., Keasling, Jay D., Simmons, Blake A., and Loqué, Dominique. 2016. "Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility". United States. https://doi.org/10.3389/fbioe.2016.00058. https://www.osti.gov/servlets/purl/1378985.
@article{osti_1378985,
title = {Expression of S-adenosylmethionine Hydrolase in Tissues Synthesizing Secondary Cell Walls Alters Specific Methylated Cell Wall Fractions and Improves Biomass Digestibility},
author = {Eudes, Aymerick and Zhao, Nanxia and Sathitsuksanoh, Noppadon and Baidoo, Edward E. K. and Lao, Jeemeng and Wang, George and Yogiswara, Sasha and Lee, Taek Soon and Singh, Seema and Mortimer, Jenny C. and Keasling, Jay D. and Simmons, Blake A. and Loqué, Dominique},
abstractNote = {Plant biomass is a large source of fermentable sugars for the synthesis of bioproducts using engineered microbes. These sugars are stored as cell wall polymers, mainly cellulose and hemicellulose, and are embedded with lignin, which makes their enzymatic hydrolysis challenging. One of the strategies to reduce cell wall recalcitrance is the modification of lignin content and composition. Lignin is a phenolic polymer of methylated aromatic alcohols and its synthesis in tissues developing secondary cell walls is a significant sink for the consumption of the methyl donor S-adenosylmethionine (AdoMet). In this study, we demonstrate in Arabidopsis stems that targeted expression of AdoMet hydrolase (AdoMetase, E.C. 3.3.1.2) in secondary cell wall synthesizing tissues reduces the AdoMet pool and impacts lignin content and composition. In particular, both NMR analysis and pyrolysis gas chromatography mass spectrometry of lignin in engineered biomass showed relative enrichment of non-methylated p-hydroxycinnamyl (H) units and a reduction of dimethylated syringyl (S) units. This indicates a lower degree of methylation compared to that in wild-type lignin. Quantification of cell wall-bound hydroxycinnamates revealed a reduction of ferulate in AdoMetase transgenic lines. Biomass from transgenic lines, in contrast to that in control plants, exhibits an enrichment of glucose content and a reduction in the degree of hemicellulose glucuronoxylan methylation. We also show that these modifications resulted in a reduction of cell wall recalcitrance, because sugar yield generated by enzymatic biomass saccharification was greater than that of wild-type plants. Considering that transgenic plants show no important diminution of biomass yields, and that heterologous expression of AdoMetase protein can be spatiotemporally optimized, this novel approach provides a valuable option for the improvement of lignocellulosic biomass feedstock.},
doi = {10.3389/fbioe.2016.00058},
url = {https://www.osti.gov/biblio/1378985}, journal = {Frontiers in Bioengineering and Biotechnology},
issn = {2296-4185},
number = ,
volume = 4,
place = {United States},
year = {Tue Jul 19 00:00:00 EDT 2016},
month = {Tue Jul 19 00:00:00 EDT 2016}
}

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Cited by: 6 works
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Works referenced in this record:

Expression of a bacterial 3-dehydroshikimate dehydratase reduces lignin content and improves biomass saccharification efficiency
journal, January 2015


Lignin Biosynthesis
journal, June 2003


CCoAOMT suppression modifies lignin composition in Pinus radiata
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Lignin bioengineering
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Hemicelluloses
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Quantitative 2D HSQC (Q-HSQC) via Suppression of J -Dependence of Polarization Transfer in NMR Spectroscopy:  Application to Wood Lignin
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4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein
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Lignin monomer composition is determined by the expression of a cytochrome P450-dependent monooxygenase in Arabidopsis
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Xylem cell death: emerging understanding of regulation and function
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Lignin modification improves fermentable sugar yields for biofuel production
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Whole plant cell wall characterization using solution-state 2D NMR
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HipA-Triggered Growth Arrest and β-Lactam Tolerance in Escherichia coli Are Mediated by RelA-Dependent ppGpp Synthesis
journal, May 2013


Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959


The maize brown midrib2 ( bm2 ) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation
journal, January 2014


Determination of S-Adenosyl-l-methionine in Fruits by Capillary Electrophoresis
journal, October 2010


SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis
journal, November 2012


Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms
journal, August 1999


Production of hydroxycinnamoyl anthranilates from glucose in Escherichia coli
journal, January 2013


Genetic transformation of strawberry: Stable integration of a gene to control biosynthesis of ethylene
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Pyrolysis-GC-MS characterization of forage materials
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Engineering secondary cell wall deposition in plants
journal, November 2012


5-Hydroxyconiferyl Aldehyde Modulates Enzymatic Methylation for Syringyl Monolignol Formation, a New View of Monolignol Biosynthesis in Angiosperms
journal, February 2000


The Folylpolyglutamate Synthetase Plastidial Isoform Is Required for Postembryonic Root Development in Arabidopsis
journal, January 2011


Efficiency of Lignin Biosynthesis: a Quantitative Analysis
journal, March 2003


Thermospermine is Not a Minor Polyamine in the Plant Kingdom
journal, February 2012


Increase in 4-Coumaryl Alcohol Units during Lignification in Alfalfa ( Medicago sativa ) Alters the Extractability and Molecular Weight of Lignin
journal, October 2010


Genetic Engineering of Cantaloupe to Reduce Ethylene Biosynthesis and Control Ripening
book, January 1999


Characterization of nonderivatized plant cell walls using high-resolution solution-state NMR spectroscopy
journal, June 2008


Modification of the degree of 4-O-methylation of secondary wall glucuronoxylan
journal, April 2014


Chemical Composition of Abaca ( Musa textilis ) Leaf Fibers Used for Manufacturing of High Quality Paper Pulps
journal, June 2006


O NE -C ARBON M ETABOLISM IN H IGHER P LANTS
journal, June 2001


Nucleotide sequence and analysis of the coliphage T3 S-adenosyhnethionine hydrolase gene and its surrounding ribonuclease III processing sites
journal, January 1987


Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis
journal, December 2015


Dual Methylation Pathways in Lignin Biosynthesis
journal, December 1998


Designer lignins: harnessing the plasticity of lignification
journal, February 2016


Aspartate-Derived Amino Acid Biosynthesis in Arabidopsis thaliana
journal, January 2009


The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase
journal, January 2015


S-Adenosyl-L-methionine: Beyond the Universal Methyl Group Donor
journal, December 2006


Characterization of nonderivatized plant cell walls using high-resolution solution-state NMR spectroscopy
journal, June 2008


Determination of S-Adenosyl-l-methionine in Fruits by Capillary Electrophoresis
journal, October 2010


Reduced ethylene synthesis by transgenic tomatoes expressing S-adenosylmethionine hydrolase
journal, November 1994


Lignin bioengineering
journal, April 2014


Designer lignins: harnessing the plasticity of lignification
journal, February 2016


Modification of the degree of 4-O-methylation of secondary wall glucuronoxylan
journal, April 2014


Use of Dinitrosalicylic Acid Reagent for Determination of Reducing Sugar
journal, March 1959


Pyrolysis-GC-MS characterization of forage materials
journal, August 1991


Chemical Composition of Abaca ( Musa textilis ) Leaf Fibers Used for Manufacturing of High Quality Paper Pulps
journal, June 2006


Lignin modification improves fermentable sugar yields for biofuel production
journal, June 2007


Whole plant cell wall characterization using solution-state 2D NMR
journal, August 2012


4-O-methylation of glucuronic acid in Arabidopsis glucuronoxylan is catalyzed by a domain of unknown function family 579 protein
journal, August 2012


Coniferyl aldehyde 5-hydroxylation and methylation direct syringyl lignin biosynthesis in angiosperms
journal, August 1999


5-Hydroxyconiferyl Aldehyde Modulates Enzymatic Methylation for Syringyl Monolignol Formation, a New View of Monolignol Biosynthesis in Angiosperms
journal, February 2000


Efficiency of Lignin Biosynthesis: a Quantitative Analysis
journal, March 2003


Xylem cell death: emerging understanding of regulation and function
journal, January 2012


SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis
journal, November 2012


Thermospermine is Not a Minor Polyamine in the Plant Kingdom
journal, February 2012


The Folylpolyglutamate Synthetase Plastidial Isoform Is Required for Postembryonic Root Development in Arabidopsis
journal, January 2011


Engineering secondary cell wall deposition in plants
journal, November 2012


Expression of a bacterial 3-dehydroshikimate dehydratase reduces lignin content and improves biomass saccharification efficiency
journal, January 2015


The maize brown midrib2 ( bm2 ) gene encodes a methylenetetrahydrofolate reductase that contributes to lignin accumulation
journal, January 2014


The maize brown midrib4 (bm4) gene encodes a functional folylpolyglutamate synthase
journal, January 2015


Hemicelluloses
journal, June 2010


O NE -C ARBON M ETABOLISM IN H IGHER P LANTS
journal, June 2001


Lignin Biosynthesis
journal, June 2003


Production of hydroxycinnamoyl anthranilates from glucose in Escherichia coli
journal, January 2013


Loss of function of folylpolyglutamate synthetase 1 reduces lignin content and improves cell wall digestibility in Arabidopsis
journal, December 2015


Aspartate-Derived Amino Acid Biosynthesis in Arabidopsis thaliana
journal, January 2009


Works referencing / citing this record:

Rhizobacteria Mediate the Phytotoxicity of a Range of Biorefinery‐Relevant Compounds
journal, July 2019